Hamish G. Spencer

Metapopulation Structure Favors Plasticity over Local Adaptation

We describe a model for the evolutionary consequences of plasticity in an environmentally heterogeneous metapopulation in which specialists for each of two alternative environments and one plastic type are initially present. The model is similar to that proposed by Moran (1992) but extends her work to two sites. We show that with migration between sites the plastic type is favored over local specialists across a broad range of parameter space. The plastic type may dominate or be fixed even in an environmentally uniform site, and even if the plasticity has imperfect accuracy or bears some cost such that a local specialist has higher fitness in that site, as long as there is some migration between sites with different distributions of environmental states. These results suggest that differences among taxa in dispersal and hence realized migration rates may play a heretofore unrecognized role in their patterns of adaptive population differentiation. Migration relaxes the thresholds for both environmental heterogeneity and accuracy of plastic response above which plasticity is favored. Furthermore, small changes in response accuracy can dramatically and abruptly alter the evolutionary outcome in the metapopulation. A fitness cost to plasticity will substantially reduce the range of conditions in which the plastic type will prevail only if the cost is both large and global rather than environment specific.

Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies

Early experience has a particularly great effect on most organisms. Normal development may be disrupted by early environmental influences; individuals that survive have to cope with the damaging consequences. Additionally, the responses required to cope with environmental challenges in early life may have long-term effects on the adult organism. A further set of processes, those of developmental plasticity, may induce a phenotype that is adapted to the adult environment predicted by the conditions of early life. A mismatch between prediction and subsequent reality can cause severe health problems in those human societies where economic circumstances and nutrition are rapidly improving. Understanding the underlying mechanisms of plasticity is, therefore, clinically important. However, to conduct research in this area, developmental plasticity must be disentangled from disruption and the adverse long-term effects of coping. The paper reviews these concepts and explores ways in which such distinctions may be made in practice.

Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum

The end of the Last Glacial Maximum (LGM) dramatically reshaped temperate ecosystems, with many species moving poleward as temperatures rose and ice receded. Whereas reinvading terrestrial taxa tracked melting glaciers, marine biota recolonized ocean habitats freed by retreating sea ice. The extent of sea ice in the Southern Hemisphere during the LGM has, however, yet to be fully resolved, with most palaeogeographic studies suggesting only minimal or patchy ice cover in subantarctic waters. Here, through population genetic analyses of the widespread Southern Bull Kelp (Durvillaea antarctica), we present evidence for persistent ice scour affecting subantarctic islands during the LGM. Using mitochondrial and chloroplast genetic markers (COI; rbcL) to genetically characterize some 300 kelp samples from 45 Southern Ocean localities, we reveal a remarkable pattern of recent recolonization in the subantarctic. Specifically, in contrast to the marked phylogeographic structure observed across coastal New Zealand and Chile (10- to 100-km scales), subantarctic samples show striking genetic homogeneity over vast distances (10,000-km scales), with a single widespread haplotype observed for each marker. From these results, we suggest that sea ice expanded further and ice scour during the LGM impacted shallow-water subantarctic marine ecosystems more extensively than previously suggested.

Phylogeographical disjunction in abundant high-dispersal littoral gastropods

Phylogeographical disjunctions in high‐dispersal marine taxa are variously ascribed to palaeogeographical conditions or contemporary ecological factors. Associated biogeographical studies, however, seldom incorporate the sampling design required to confidently discriminate among such competing hypotheses. In the current study, over 7800 gastropod specimens were examined for operculum colour, and 129 specimens genetically, to test ecological and historical biogeographical hypotheses relating to biogeographical disjunction in the Southern Hemisphere, and to southern Australia in particular. Mitochondrial DNA sequence analysis of the high‐dispersal intertidal gastropod Nerita atramentosa in southern Australia (88 specimens; 18 localities) revealed an east–west phylogeographical split involving two highly divergent clades (26.0 ± 1.9%) exhibiting minimal geographical overlap in the southeast. The eastern clade of Nerita atramentosa is also widespread in northern New Zealand (43 specimens, 10 localities), but no significant genetic differentiation is explained by the Tasman Sea, a 2000‐km‐wide oceanic barrier. Spatial genetic structure was not detected within either clade, consistent with the species’ dispersive planktotrophic phase lasting for 5–6 months. Digital analysis of operculum colouration revealed substantial differences between eastern (tan) and western (black) specimens. Genetic analysis and visual inspection of 88 Australian specimens revealed a completely nonrandom association between mtDNA data and operculum colouration. Independent examination of a further 7822 specimens from 14 sites in southern Australia revealed both colour morphs at all localities, but reinforced the phylogeographical data by indicating a marked turnover in colour morph abundance associated with a palaeogeographical barrier: Wilsons Promontory. This sharp biogeographical disjunction is in marked contrast to the species’ high dispersal abilities. The genetic similarity of Nerita morio (Easter Island) and the eastern Australian + New Zealand lineage (1.1 ± 0.3%) provides further evidence of long‐distance dispersal in southern Nerita. Phylogenetic relationships of nine species (four genera) of Neritidae, an almost exclusively tropical gastropod family, are consistent with the hypothesis that southern temperate black nerites comprise a monophyletic radiation.

Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp

BackgroundSouth Americas western coastline, extending in a near-straight line across some 35 latitudinal degrees, presents an elegant setting for assessing both contemporary and historic influences on cladogenesis in the marine environment. Southern bull-kelp (Durvillaea antarctica) has a broad distribution along much of the Chilean coast. This species represents an ideal model taxon for studies of coastal marine connectivity and of palaeoclimatic effects, as it grows only on exposed rocky coasts and is absent from beaches and ice-affected shores. We expected that, along the central Chilean coast, D. antarctica would show considerable phylogeographic structure as a consequence of the isolating effects of distance and habitat discontinuities. In contrast, we hypothesised that further south - throughout the region affected by the Patagonian Ice Sheet at the Last Glacial Maximum (LGM) - D. antarctica would show relatively little genetic structure, reflecting postglacial recolonisation.ResultsMitochondrial (COI) and chloroplast (rbcL) DNA analyses of D. antarctica from 24 Chilean localities (164 individuals) revealed two deeply divergent (4.5 - 6.1% for COI, 1.4% for rbcL) clades from the centre and south of the country, with contrasting levels and patterns of genetic structure. Among populations from central Chile (32° - 44°S), substantial phylogeographic structure was evident across small spatial scales, and a significant isolation-by-distance effect was observed. Genetic disjunctions in this region appear to correspond to the presence of long beaches. In contrast to the genetic structure found among central Chilean populations, samples from the southern Chilean Patagonian region (49° - 56°S) were genetically homogeneous and identical to a haplotype recently found throughout the subantarctic region.ConclusionsSouthern (Patagonian) Chile has been recolonised by D. antarctica relatively recently, probably since the LGM. The inferred trans-oceanic ancestry of these Patagonian populations supports the notion that D. antarctica is capable of long-distance dispersal via rafting. In contrast, further north in central Chile, the correspondence of genetic disjunctions in D. antarctica with long beaches indicates that habitat discontinuity drives genetic isolation among established kelp populations. We conclude that rafting facilitates colonisation of unoccupied shores, but has limited potential to enhance gene-flow among established populations. Broadly, this study demonstrates that some taxa may be considered to have either high or low dispersal potential across different temporal and geographic scales.

A theoretical investigation of speciation by reinforcement

The reinforcement model of speciation holds an important place in modern evolutionary thought. A closer examination of the model using a computer simulation reveals that there are a number of implicit assumptions necessary for reinforcement to work. 1. It requires that reproductive characters form part of an open genetic system with high heritability and that there is considerable variability within this system. 2. The two strains must coexist throughout the period in which selection is acting. This requires intense frequency-dependent selection to counteract the inherently unstable selection regime of negative heterosis. The necessary intensity suggests that extinction of one of the strains is the more likely outcome unless there are substantial initial differences in reproductive characters. Furthermore, chance extinction of one of the strains cannot occur in this selection period. 3. The net cost of assortative characters must be less than the cost of a greater probability of producing hybrid offspring. This is a complex matter with several opposing factors. 4. The fitness of the hybrids must be zero or close to it and must remain so. 5. The selective pressure for assortative reproductive characters becomes weaker as these characters are established. It appears unlikely that selection alone could complete the process, as is hypothesized in some formulations of the model. Further data from natural populations and laboratory experiments are required to clarify several of these points, especially the first. These problems do not mean that reinforcement can never occur, but they do imply that speciation by reinforcement is not nearly as prevalent as much of the biological literature suggests.

Comparative and meta‐analytic insights into life extension via dietary restriction

Dietary restriction (DR) extends the lifespan of a wide range of species, although the universality of this effect has never been quantitatively examined. Here, we report the first comprehensive comparative meta‐analysis of DR across studies and species. Overall, DR significantly increased lifespan, but this effect is modulated by several factors. In general, DR has less effect in extending lifespan in males and also in non‐model organisms. Surprisingly, the proportion of protein intake was more important for life extension via DR than the degree of caloric restriction. Furthermore, we show that reduction in both age‐dependent and age‐independent mortality rates drives life extension by DR among the well‐studied laboratory model species (yeast, nematode worms, fruit flies and rodents). Our results suggest that convergent adaptation to laboratory conditions better explains the observed DR–longevity relationship than evolutionary conservation although alternative explanations are possible.

HOW STABLE ‘SHOULD’ EPIGENETIC MODIFICATIONS BE? INSIGHTS FROM ADAPTIVE PLASTICITY AND BET HEDGING

Although there is keen interest in the potential adaptive value of epigenetic variation, it is unclear what conditions favor the stability of these variants either within or across generations. Because epigenetic modifications can be environmentally sensitive, existing theory on adaptive phenotypic plasticity provides relevant insights. Our consideration of this theory suggests that stable maintenance of environmentally induced epigenetic states over an organisms lifetime is most likely to be favored when the organism accurately responds to a single environmental change that subsequently remains constant, or when the environmental change cues an irreversible developmental transition. Stable transmission of adaptive epigenetic states from parents to offspring may be selectively favored when environments vary across generations and the parental environment predicts the offspring environment. The adaptive value of stability beyond a single generation of parent–offspring transmission likely depends on the costs of epigenetic resetting. Epigenetic stability both within and across generations will also depend on the degree and predictability of environmental variation, dispersal patterns, and the (epi)genetic architecture underlying phenotypic responses to environment. We also discuss conditions that favor stability of random epigenetic variants within the context of bet hedging. We conclude by proposing research directions to clarify the adaptive significance of epigenetic stability.

CLADOGENESIS AS THE RESULT OF LONG-DISTANCE RAFTING EVENTS IN SOUTH PACIFIC TOPSHELLS (GASTROPODA, TROCHIDAE)

Abstract We used DNA sequences of lecithotrophic monodontine topshells, belonging to the genera Diloma, Melagraphia, and Austrocochlea, to ascertain how this group became established over a large area of the South Pacific Ocean. The phylogeny of the topshells was estimated using portions of two mitochondrial genes (16S and cytochrome oxidase 1) and one nuclear gene (actin). A range of divergence rates was used to estimate the approximate timing of cladogenetic events within their phylogenetic tree. These estimates allow us to unambiguously reject vicariant explanations for several major divergence events and to infer several dispersal events across wide stretches of ocean. The first were two initial dispersal events from Australia (1) to an area between Samoa and Japan and (2) to New Zealand. Subsequently, at least one, and possibly two, recent eastward dispersals took place from New Zealand to Chile and the Juan Fernandez Islands, and one further dispersal occurred from somewhere in the tropical Pacific to Samoa. Moreover, owing to the short‐lived nature of the topshell larvae, transoceanic larval dispersal is unlikely. The apparent paradox of a short larval phase and broad geographic range suggests that dispersal most probably occurred by rafting of adults on a suitable platform such as macroalgae; indeed, naturally buoyant bull kelp is the natural habitat of the most geographically widespread species in this group. Our molecular phylogenies imply that, despite of being an unlikely event, adult rafting in ocean currents has occurred on several occasions throughout the evolutionary history of topshells, resulting in their wide present‐day distribution.

Predictive adaptive responses in perspective

In a recent opinion article, Wells accepts our fundamental claim that early metabolic plasticity in humans can contribute to later disease if there is a disparity (‘mismatch’) between nutritional experience at different phases of life, but he revives a debate and about the nature and function of the cue directing such plasticity. As in that earlier exchange, Wells argues that (i) the interests of mother and offspring are distinct, (ii) the only traits of interest are nutritional and metabolic and (iii) modern humans are in some way ‘special’ because of their extended lifespan and reproductive strategy. He argues that in humans prediction has been abandoned for a backward-looking strategy that operates solely for maternal benefit. We have explained elsewhere why we do not believe this to be the case. We suggest that a broader approach is needed because (i) evolution maximizes inclusive fitness, requiring optimization of the outcomes of the set of maternofetal dyads produced across the mothers reproductive life, (ii) plasticity cued by early-life information operates through trade-offs among the whole suite of life-history traits, and it is misleading to concentrate on a single trait and (iii) as in other species, humans use the mechanisms of developmental plasticity cued by information from the past and the present to prepare for the future.